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Inhibition of gametogenesis by the cestode Ligula intestinalis in roach (Rutilus rutilus) is attenuated under laboratory conditions

Published online by Cambridge University Press:  22 November 2010

ACHIM TRUBIROHA ,
HANA KROUPOVA ,
SABRINA N. FRANK ,
BERND SURES  and
WERNER KLOAS
ACHIM TRUBIROHA*
Affiliation:
Department of Ecophysiology and Aquaculture, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Mueggelseedamm 310, D-12587 Berlin, Germany
HANA KROUPOVA
Affiliation:
Department of Ecophysiology and Aquaculture, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Mueggelseedamm 310, D-12587 Berlin, Germany Research Institute of Fish Culture and Hydrobiology, Faculty of Fisheries and Protection of Waters, University of South Bohemia in Ceske Budejovice, Zatisi 728/II, 38925 Vodnany, Czech Republic
SABRINA N. FRANK
Affiliation:
Department of Ecophysiology and Aquaculture, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Mueggelseedamm 310, D-12587 Berlin, Germany Department of Applied Zoology/Hydrobiology, University of Duisburg/Essen, Universitaetsstrasse 5, D-45141 Essen, Germany
BERND SURES
Affiliation:
Department of Applied Zoology/Hydrobiology, University of Duisburg/Essen, Universitaetsstrasse 5, D-45141 Essen, Germany
WERNER KLOAS
Affiliation:
Department of Ecophysiology and Aquaculture, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Mueggelseedamm 310, D-12587 Berlin, Germany Department of Endocrinology, Humboldt University Berlin, Invalidenstrasse 42, D-10099 Berlin, Germany
*
*Corresponding author: Department of Ecophysiology and Aquaculture, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Mueggelseedamm 301, D-12587 Berlin, Germany. Tel: +49 30 64181 614. Fax: +49 30 64181 799. E-mail: trubiroha@igb-berlin.de
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Summary

Reproductive parameters of Ligula intestinalis-infected roach (Rutilus rutilus) which were held under long-tem laboratory conditions with unlimited food supply were investigated. Although uninfected and infected roach showed no difference in condition factor and both groups deposited perivisceral fat, the gonadosomatic-index was significantly lower in infected female and male roach. Quantitative histological analysis revealed that gonad development was retarded upon parasitization in both genders. In contrast to the phenotype described in the field, infected females were able to recruit follicles into secondary growth, but a high percentage of secondary growth follicles underwent atresia. In both genders, the histological data corresponded well with reduced expression of pituitary gonadotropins and lowered plasma concentrations of sex steroids, as revealed by real-time RT-PCR and ELISA, respectively. Furthermore, a reduction of vitellogenin mRNA and modulated expression of sex steroid receptors in the liver was demonstrated. Like in the field, there was a significant adverse impact of L. intestinalis on host reproductive physiology which could not be related to parasite burden. Our results show, for the first time, that maintenance under laboratory conditions can not abolish the deleterious effect of L. intestinalis on gametogenesis in roach, and indicate a specific inhibition of host reproduction by endocrine disruption.

Keywords

parasitetapewormhost fecundityparasitic castrationendocrine disruptiongonadotropinsex steroidsoestrogenandrogenvitellogenin
Type
Research Article
Information
Parasitology , Volume 138 , Issue 5 , April 2011 , pp. 648 - 659
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Andersen, L., Goto-Kazeto, R., Trant, J. M., Nash, J. P., Korsgaard, B. and Bjerregaard, P. (2006). Short-term exposure to low concentrations of the synthetic androgen methyltestosterone affects vitellogenin and steroid levels in adult male zebrafish (Danio rerio). Aquatic Toxicology 76, 343–352.CrossRefGoogle ScholarPubMed
Arme, C. (1968). Effects of plerocercoid larva of a pseudophyllidean cestode Ligula intestinalis on pituitary gland and gonads of its host. Biological Bulletin 134, 15–25.CrossRefGoogle Scholar
Arme, C. (1997). Ligula intestinalis: interactions with the pituitary-gonadal axis of its fish host. Journal of Helminthology 71, 83–84.CrossRefGoogle Scholar
Arme, C. and Owen, R. W. (1968). Occurrence and pathology of Ligula intestinalis infections in British fishes. Journal of Parasitology 54, 272–280.CrossRefGoogle ScholarPubMed
Bagamian, K. H., Heins, D. C. and Baker, J. A. (2004). Body condition and reproductive capacity of three-spined stickleback infected with the cestode Schistocephalus solidus. Journal of Fish Biology 64, 1568–1576.CrossRefGoogle Scholar
Barber, I. and Svensson, P. A. (2003). Effects of experimental Schistocephalus solidus infections on growth, morphology and sexual development of female three-spined sticklebacks, Gasterosteus aculeatus. Parasitology 126, 359–367.CrossRefGoogle ScholarPubMed
Barber, I., Wright, H. A., Arnott, S. A. and Wootton, R. J. (2008). Growth and energetics in the stickleback-Schistocephalus host-parasite system: a review of experimental infection studies. Behaviour 145, 647–668.Google Scholar
Campbell, B., Dickey, J., Beckman, B., Young, G., Pierce, A., Fukada, H. and Swanson, P. (2006). Previtellogenic oocyte growth in salmon: relationships among body growth, plasma insulin-like growth factor-1, estradiol-17beta, follicle-stimulating hormone and expression of ovarian genes for insulin-like growth factors, steroidogenic-acute regulatory protein and receptors for gonadotropins, growth hormone, and somatolactin. Biology of Reproduction 75, 34–44.CrossRefGoogle ScholarPubMed
Candolin, U. and Voigt, H. R. (2001). No effect of a parasite on reproduction in stickleback males: a laboratory artefact? Parasitology 122, 457–464.CrossRefGoogle Scholar
Carter, V., Pierce, R., Dufour, S., Arme, C. and Hoole, D. (2005). The tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea) inhibits LH expression and puberty in its teleost host, Rutilus rutilus. Reproduction 130, 939–945.CrossRefGoogle ScholarPubMed
Dubinina, M. N. (1980). Tapeworms (Cestoda, Ligulidae) of the Fauna of the U.S.S.R. Amerind Publishing Co., New Delhi, India.Google Scholar
Ebert, D., Carius, H. J., Little, T. and Decaestecker, E. (2004). The evolution of virulence when parasites cause host castration and gigantism. American Naturalist 164, 19–32.CrossRefGoogle ScholarPubMed
Ewald, P. W. (1980). Evolutionary biology and the treatment of signs and symptoms of infectious disease. Journal of Theoretical Biology 86, 169–176.CrossRefGoogle ScholarPubMed
Filby, A. L. and Tyler, C. R. (2005). Molecular characterization of estrogen receptors 1, 2a, and 2b and their tissue and ontogenic expression profiles in fathead minnow (Pimephales promelas). Biology of Reproduction 73, 648–662.CrossRefGoogle ScholarPubMed
Geraudie, P., Boulange-Lecomte, C., Gerbron, M., Hinfray, N., Brion, F. and Minier, C. (2010). Endocrine effects of the tapeworm Ligula intestinalis in its teleost host, the roach (Rutilus rutilus). Parasitology 137, 697–704.CrossRefGoogle ScholarPubMed
Hall, S. R., Becker, C. and Caceres, C. E. (2007). Parasitic castration: a perspective from a model of dynamic energy budgets. Integrative and Comparative Biology 47, 295–309.CrossRefGoogle Scholar
Hecker, M. and Karbe, L. (2005). Parasitism in fish – an endocrine modulator of ecological relevance? Aquatic Toxicology 72, 195–207.CrossRefGoogle Scholar
Heins, D. C. and Baker, J. A. (2003). Reduction of egg size in natural populations of threespine stickleback infected with a cestode macroparasite. Journal of Parasitology 89, 1–6.CrossRefGoogle ScholarPubMed
Heins, D. C. and Baker, J. A. (2008). The stickleback-Schistocephalus host-parasite system as a model for understanding the effect of a macroparasite on host reproduction. Behaviour 145, 625–645.CrossRefGoogle Scholar
Heins, D. C. and Brown-Peterson, N. J. (2010). Influence of the pseudophyllidean cestode Schistocephalus solidus on oocyte development in the threespine stickleback Gasterosteus aculeatus. Parasitology 137, 1151–1158.CrossRefGoogle ScholarPubMed
Heins, D. C., Baker, J. A., Toups, M. A. and Birden, E. L. (2010). Evolutionary significance of fecundity reduction in threespine stickleback infected by the diphyllobothriidean cestode Schistocephalus solidus. Biological Journal of the Linnean Society 100, 835–846.CrossRefGoogle Scholar
Hoole, D., Carter, V. and Dufour, S. (2010). Ligula intestinalis (Cestoda: Pseudophyllidea): an ideal fish-metazoan parasite model? Parasitology 137, 425–438.CrossRefGoogle ScholarPubMed
Huertas, M., Scott, A. P., Hubbard, P. C., Canario, A. V. and Cerda, J. (2006). Sexually mature European eels (Anguilla anguilla L.) stimulate gonadal development of neighbouring males: possible involvement of chemical communication. General and Comparative Endocrinology 147, 304–313.CrossRefGoogle ScholarPubMed
Hurd, H. (2001). Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363–368.CrossRefGoogle ScholarPubMed
Hurd, H. (2009). Evolutionary drivers of parasite-induced changes in insect life-history traits: From theory to underlying mechanisms. Advances in Parasitology 68, 85–110.CrossRefGoogle ScholarPubMed
Katsu, Y., Lange, A., Urushitani, H., Ichikawa, R., Paull, G. C., Cahill, L. L., Jobling, S., Tyler, C. R. and Iguchi, T. (2007). Functional associations between two estrogen receptors, environmental estrogens, and sexual disruption in the roach (Rutilus rutilus). Environmental Science and Technology 41, 3368–3374.CrossRefGoogle ScholarPubMed
Kloas, W., Urbatzka, R., Opitz, R., Wuertz, S., Behrends, T., Hermelink, B., Hofmann, F., Jagnytsch, O., Kroupova, H., Lorenz, C., Neumann, N., Pietsch, C., Trubiroha, A., Van Ballegooy, C., Wiedemann, C. and Lutz, I. (2009). Endocrine disruption in aquatic vertebrates. Annals of the New York Academy of Sciences 1163, 187–200.CrossRefGoogle ScholarPubMed
Lafferty, K. D. and Kuris, A. M. (2009). Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitology 25, 564–572.CrossRefGoogle ScholarPubMed
Lange, A., Katsu, Y., Ichikawa, R., Paull, G. C., Chidgey, L. L., Coe, T. S., Iguchi, T. and Tyler, C. R. (2008). Altered sexual development in roach (Rutilus rutilus) exposed to environmental concentrations of the pharmaceutical 17alpha-ethinylestradiol and associated expression dynamics of aromatases and estrogen receptors. Toxicological Sciences 106, 113–123.CrossRefGoogle ScholarPubMed
Leanos-Castaneda, O. and Van De Kraak, G. (2007). Functional characterization of estrogen receptor subtypes, ERalpha and ERbeta, mediating vitellogenin production in the liver of rainbow trout. Toxicology and Applied Pharmacology 224, 116–125.CrossRefGoogle ScholarPubMed
Levavi-Sivan, B., Bogerd, J., Mananos, E. L., Gomez, A. and Lareyre, J. J. (2010). Perspectives on fish gonadotropins and their receptors. General and Comparative Endocrinology 165, 412–437.CrossRefGoogle ScholarPubMed
Li, Z., Zhang, S. and Liu, Q. (2008). Vitellogenin functions as a multivalent pattern recognition receptor with an opsonic activity. PLoS ONE 3, e1940.CrossRefGoogle ScholarPubMed
Loot, G., Brosse, S., Lek, S. and Guegan, J. F. (2001). Behaviour of roach (Rutilus rutilus L.) altered by Ligula intestinalis (Cestoda: Pseudophyllidea): a field demonstration. Freshwater Biology 46, 1219–1227.CrossRefGoogle Scholar
Lower, N., Scott, A. P. and Moore, A. (2004). Release of sex steroids into the water by roach. Journal of Fish Biology 64, 16–33.CrossRefGoogle Scholar
Lubzens, E., Young, G., Bobe, J. and Cerda, J. (2010). Oogenesis in teleosts: how eggs are formed. General and Comparative Endocrinology 165, 367–389.CrossRefGoogle ScholarPubMed
MacNab, V., Katsiadaki, I. and Barber, I. (2009). Reproductive potential of Schistocephalus solidus-infected male three-spined stickleback Gasterosteus aculeatus from two UK populations. Journal of Fish Biology 75, 2095–2107.CrossRefGoogle Scholar
Menuet, A., Le Page, Y., Torres, O., Kern, L., Kah, O. and Pakdel, F. (2004). Analysis of the estrogen regulation of the zebrafish estrogen receptor (ER) reveals distinct effects of ERalpha, ERbeta1 and ERbeta2. Journal of Molecular Endocrinology 32, 975–986.CrossRefGoogle ScholarPubMed
Nelson, E. R. and Habibi, H. R. (2010). Functional significance of nuclear estrogen receptor subtypes in the liver of goldfish. Endocrinology 151, 1668–1676.CrossRefGoogle ScholarPubMed
Nolan, M., Jobling, S., Brighty, G., Sumpter, J. P. and Tyler, C. R. (2001). A histological description of intersexuality in the roach. Journal of Fish Biology 58, 160–176.CrossRefGoogle Scholar
Orr, T. S. C. (1966). Spawning behaviour of rudd Scardinius erythrophthalmus infested with plerocercoids of Ligula intestinalis. Nature, London 212, 736.CrossRefGoogle Scholar
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Rinchard, J. and Kestemont, P. (1996). Comparative study of reproductive biology in single- and multiple-spawner cyprinid fish. 1. Morphological and histological features. Journal of Fish Biology 49, 883–894.Google Scholar
Schulz, R. W., de Franca, L. R., Lareyre, J-J., LeGac, F., Chiarini-Garcia, H., Nobrega, R. H. and Miura, T. (2010). Spermatogenesis in fish. General and Comparative Endocrinology 165, 390–411.CrossRefGoogle ScholarPubMed
Schultz, E. T., Topper, M. and Heins, D. C. (2006). Decreased reproductive investment of female threespine stickleback Gasterosteus aculeatus infected with the cestode Schistocephalus solidus: parasite adaptation, host adaptation, or side effect? Oikos 114, 303–310.CrossRefGoogle Scholar
Smith, V. (2007). Host resource supplies influence the dynamics and outcome of infectious disease. Integrative and Comparative Biology 47, 310–316.CrossRefGoogle ScholarPubMed
Tierney, J. F., Huntingford, F. A. and Crompton, D. W. T. (1996). Body condition and reproductive status in sticklebacks exposed to a single wave of Schistocephalus solidus infection. Journal of Fish Biology 49, 483–493.Google Scholar
Trubiroha, A., Kroupova, H., Wuertz, S., Frank, S. N., Sures, B. and Kloas, W. (2010). Naturally-induced endocrine disruption by the parasite Ligula intestinalis (Cestoda) in roach (Rutilus rutilus). General and Comparative Endocrinology 166, 234–240.CrossRefGoogle ScholarPubMed
Trubiroha, A., Wuertz, S., Frank, S. N., Sures, B. and Kloas, W. (2009). Expression of gonadotropin subunits in roach (Rutilus rutilus, Cyprinidae) infected with plerocercoids of the tapeworm Ligula intestinalis (Cestoda). International Journal for Parasitology 39, 1465–1473.CrossRefGoogle ScholarPubMed
Van Weerd, J. H., Sukkel, M., Bongers, A. B., Van der Does, H. M., Steynis, E. and Richter, C. J. (1991). Stimulation of gonadal development by sexual interaction of pubertal African catfish, Clarias gariepinus. Physiology and Behaviour 49, 217–223.CrossRefGoogle ScholarPubMed
Wahli, W. (1988). Evolution and expression of vitellogenin genes. Trends in Genetics 4, 227–232.CrossRefGoogle ScholarPubMed
Wood, A. W. and Van der Kraak, G. (2002). Inhibition of apoptosis in vitellogenic ovarian follicles of rainbow trout (Oncorhynchus mykiss) by salmon gonadotropin, epidermal growth factor, and 17beta-estradiol. Molecular Reproduction and Development 61, 511–518.CrossRefGoogle ScholarPubMed